Art 14 Bai y Rai 2011 Bacterial Quorum Sensing and Food Industry PDF

Bacterial Quorum Sensing and Food Industry
A. Jamuna Bai and V. Ravishankar Rai
Abstract: Food spoilage and biofilm formation by food-related bacteria are significant problems in the food industry.
Even with the application of modern-day food preservative techniques, excessive amounts of food are lost due to
microbial spoilage. A number of studies have indicated that quorum sensing plays a major role in food spoilage,
biofilm formation, and food-related pathogenesis. Understanding bacterial quorum-sensing signaling systems can help
in controlling the growth of undesirable food-related bacteria. This review focusses on the various signaling molecules
produced by Gram-negative and Gram-positive bacteria and the mechanism of their quorum-sensing systems, types of
signaling molecules that have been detected in different food systems using biosensors, the role of signaling molecules
in biofilm formation, and significance of biofilms in the food industry. As quorum-sensing signaling molecules are
implicated in food spoilage, based on these molecules potential, quorum-sensing inhibitors/antagonists can be developed
to be used as novel food preservatives for maintaining food integrity and enhancing food safety.
Practical Application: Bacteria use signaling molecules for inter- and intracellular communication. This phenomenon of bacterial cell-to-cell communication is known as quorum sensing. Quorum-sensing signals are implicated
in bacterial pathogenicity and food spoilage. Therefore, blocking the quorum-sensing signaling molecules in food-related
bacteria may possibly prevent quorum-sensing-regulated phenotypes responsible for food spoilage. Quorum-sensing
inhibitors/antagonists could be used as food preservatives to enhance the shelf life and also increase food safety.
Introduction
cell communication is employed by a diverse group of bacteria

including those commonly associated with food to communicate
with each other by producing the signaling molecules, autoinducers. Through the mechanisms of quorum sensing, bacteria are able
to express specific genes in response to population density. It is possible that the bacterial spoilage of some food products is influenced
by quorum-sensing-regulated phenotypes. Further studies on the
possible role of quorum-sensing compounds in food spoilage reactions can lead to the development of novel preservation techniques
based on potential quorum-sensing inhibitors.
Quorum sensing has been extensively studied in bacterial
pathogenicity (Smith and others 2004), and now it is implicated
that quorum sensing could be involved in bacterial food spoilage.
Several proteolytic, lipolytic, chitinolytic, and pectinolytic activities associated with the deterioration of foods are regulated by
quorum sensing. Moreover, several types of signaling molecules
have been detected in different spoiled food products. Hence,
disrupting the quorum-sensing circuit can play a major role in
controlling microbial gene expression related to human infection and food spoilage. The role of quorum-sensing signaling
molecules involved in food spoilage needs to be understood to
block the causative cell-to-cell communication and prevent microbial spoilage. Quorum-sensing inhibitors can be developed that
MS 20101264 Submitted 11/8/2010, Accepted 1/28/2011. Authors are with
Dept. of Studies in Microbiology, Univ. of Mysore, Manasagangotri, Mysore 570006, target synthesis of the cell signaling molecules or block these
signaling systems that can lead to prevention of food spoilage and
India. Direct inquiries to author Rai (E-mail: raivittal@gmail.com).
biofilm formation by food-related bacteria.
Food spoilage is a complex process. It is caused by the various

biochemical changes naturally occurring in foods and due to microbial activities. Microbial spoilage is the most common cause of
spoilage (Gram and others 2002). Excessive amount of foods are
lost due to microbial spoilage. It is a major concern in the food industry as it causes significant economic losses and can have serious
public health consequences (Kumar and Anand 1998). Microbial
food spoilage manifests itself as visible growth and food textural
changes (Gram and others 2002).The off-taste and off-odor due to
release of metabolites by microbes results in rejection of the food.
Microorganisms produce saccharolytic, proteolytic, pectinolytic,
and lipolytic enzymes whose metabolic end products are associated with food spoilage (Braun and others 1999; Loureiro 2000;
Ragaert and others 2007). Thus, microbial activity is considered to
be of great importance for the manifestation of spoilage (Nychas
and others 2006, 2007). In recent years, the detection of quorumsensing signals in spoiled food products has added a new dimension
to study the process of food spoilage. Quorum sensing or cell-to-
184 Comprehensive Reviews in Food Science and Food Safety r Vol. 10, 2011

c 2011 Institute of Food Technologists
doi 10.1111/j.1541-4337.2011.00150.x
Bacterial quorum sensing . . .

The aim of this review is to understand the mechanism of quorum sensing in food spoilage and by foodborne bacteria, assess
the role of signaling molecules in food spoilage and pathogenicity of food-related bacteria, and to exploit potential quorumsensing inhibitors as food preservatives to delay or prevent food
spoilage.
Quorum Sensing
One of the most remarkable discoveries in microbiology in the
past 30 y has been the fact that bacterial cells communicate with
each other. In bacteria, cell-to-cell communication is a wide spread
phenomenon controlling a broad range of activities. The modulation of gene expression in bacteria by quorum sensing results
in phenotypic changes leading to their better adjustment to environmental conditions during growth (Turovskiy and others 2007).
Cell-to-cell communication depends on the production of, secretion of, and response to small, diffusible signal molecules called
autoinducers. The signal molecules are produced and secreted at
a basal level during bacterial growth. Their concentration in the
environmental medium or matrix increases as the bacterial population expands, and when it reaches a threshold level (quorum
level), it induces phenotypic effects by regulating quorum-sensingdependent target gene expression (Czajkowski and Jafra 2009).
This phenomenon occurs without any external intervention and
is also referred to as autoinduction (Nealson and others 1970).
The cell-to-cell communication has been aptly termed quorum
sensing by Fuqua and Winans (1994). The various processes modulated by quorum sensing are usually tuned for damage to bacteria
and their survival under stressful conditions. Quorum sensing is
involved mainly in the regulation of virulence, development of
genetic competence, transfer of conjugative plasmids, sporulation,
biofilm formation, antimicrobial peptide synthesis, and symbiosis
(Smith and others 2004).
There are 2 groups of signal molecules involved in bacterial
quorum sensing. One is the peptide derivatives typically used
by Gram-positive bacteria, while the fatty acid derivatives are
exploited by the Gram-negative bacteria. Quorum sensing is
omnipresent in many known bacterial species. Many human
and plant pathogenic Gram-negative bacteria, including the
genera Agrobacterium, Brucella, Bukholderia, Erwinia, Enterobacter,
Pseudomonas, Ralstonia, Serratia, Vibrio, and Yersinia exploit the
quorum-sensing mechanism for the regulation of virulence factors
syntheses (Williams 2007). Bacteria from the genera Bacillus,
Enterococcus, Staphylococcus, Streptococcus, and Streptomyces utilize this
mechanism to develop genetic competence, produce antimicrobial
peptides or exotoxins, and for biofilm formation (Podbielski and
Kreikemeyer 2004). The Rhizobium genus uses quorum sensing for
nitrogen fixation. In these symbiotic bacteria, the nodulation and
symbiosome development required for nitrogen fixation is under
complex quorum-sensing regulatory systems (Hoang and others
2004). Quorum sensing has also been observed in extremophiles
such as the haloalkaliphilic archeon Natronococcus occultus and the
Halomonas genus of bacteria (Paggi and others 2003; Llamas and
others 2005), in the hyperthermophilic bacterium Thermotoga
maritima (Johnson and others 2005), and in Acidithiobacillus
ferrooxidans (Rivas and others 2007), an acidophilic bacterium.
Mechanisms of Quorum Sensing

Most bacteria utilize 2 general mechanisms for detecting and
responding to quorum-sensing signals. These 2 quorum-sensing

systems are used in modulating the target gene expression. One

mechanism is represented by acylhomoserine lactone (AHL) dependent quorum-sensing systems. Here, the quorum-sensing signal is detected by a cytosolic transcription factor. In the other
mechanism, the quorum-sensing signal, such as the autoinducing peptide (AIP) produced by Staphylococcus aureus, is detected by
a membrane-associated 2-component response regulatory system
(Dong and others 2005). However, the quorum-sensing circuit of
Vibrio harveyi has features of both the Gram-negative and Grampositive quorum-sensing systems. Similar to other Gram-negative
bacteria, V. harveyi produces and responds to acylated homoserine lactone (HSL), but analogus to the Gram-positive bacteria
the quorum-sensing signal transduction occurs by the membranebound histidine kinases (Waters and Bassler 2005).
In AHL-mediated quorum sensing, bacteria synthesize AHL
molecules using S-adenosylmethionine (SAM) and acyl chains
derived from the common fatty acid biosynthesis pathway. AHL
synthase (I-protein) encoded by LuxI homologue synthesizes AHL
molecules (More and others 1996; Schaefer and others 1996).
During low bacterial population density, each cell produces a
basal level of AHL signal. The short-chain AHL signal passively
diffuses across bacterial membranes and accumulates in the environment (Pearson and others 1999; Dong and others 2005). But
the long-chain AHL signals require active transportation mechanisms for their efflux (Chan and Chua 2005). One such example is
Pseudomonas aeruginosa that uses multidrug efflux pump MexABOprM for the active transport of 3-oxo-C12 HSL signal (Pearson
and others 1999). With an increase in bacterial population, the
concentration of AHL signal reaches a threshold level, resulting
in signal accumulation and recognition by the cognate receptors.
The signal reception involves R protein. These R proteins belong to the Lux R family of transcriptional regulators and act
as receptors for the AHLs synthesized by the LuxI proteins. The
R-AHL complex, which is a dimer, binds to conserved palindromic sequences of the quorum-controlled promoters, including
the promoter of the luxI-type gene, and boosts AHL production
(autoinduction) and expression of other genes in the quorumsensing regulon (Schuster and others 2004). Thus, the R-AHL
complex is involved in autoinduction and control of quorumsensing regulons. The AHL-degradation enzyme and the cognate
regulatory transcription factor(s) are involved in signal decay. The
AHL-degradation enzymes have been identified in several bacterial pathogens that produce AHL signals, such as Agrobacterium
tumefaciens and P. aeruginosa (Huang and others 2003). The degradation of AHL signals switches off the quorum-sensing-dependent
gene expression (Zhang and others 2004).
AHL-mediated quorum sensing is one of the best characterized cell-to-cell communication mechanisms (Table 1). It is used
by many bacterial species among which are, the agriculturally
important A. tumefaciens and Erwinia carotovora and the medically
important P. aeruginosa and Burkholderia species (Dong and others
2000; Williams 2007).
The 2-component system mediated quorum sensing is present
in both Gram-positive and Gram-negative bacteria (Waters and
Bassler 2005). Here, the quorum-sensing signal, such as the
AIP signal, is transported to the intercellular environment by an
ABC transporter. The accumulated signals are detected by a 2component sensor that transfers the sensory information to activate a cognate response regulator for modulating the expression of
quorum-sensing regulon through regulatory RNAs and intracellular transcription factors (Novick 2003). There are no reports on
signal decay in the AIP-type quorum-sensing process.
Vol. 10, 2011 r Comprehensive Reviews in Food Science and Food Safety 185

Table 1Mechanism of AHL-type quorum-sensing systems.
Quorum sensing process
At low population density,
AHL synthase uses
S-adenosylmethionine
(SAM) and acyl chains to
synthesize AHL.
Short-chain AHLs diffuse
passively.
Long-chain signals require
active efflux.
At high population density,
LuxR-type (R) transcription
factor recognizes signal.
R proteins and AHLs bind to
target DNA leading to
increased AHL signal
production and activation
of quorum-sensing regulon.
Outcome
Signal generation
Signal accumulation
Signal reception
Autoinduction
Quorum-Sensing Signals
RhlI/RhlR, adding an additional level of control through AHL

signaling (de Kievit and Iglewski 2000). Earlier it was assumed that
References
bacteria use quorum-sensing systems to monitor their population
Schaefer and others
density, but studies on Escherichia coli (E. coli) and Salmonella Ty(1996)
phimurium show that this is not always the case. EC and Salmonella
enterica serovar Typhimurium (S. Typhimurium), for example, do
not have a LuxI homologue and therefore do not produce any AIDong and others
(2005)
1, but they do encode a LuxR homologue named SdiA that when
overexpressed has been shown to have a negative effect on genes
Schuster and others involved in cell attachment in enterohemorrhagic EC (EHEC)
(2004)
(Kanamaru and others 2000), but positively regulates several genes
located on the S. Typhimurium virulence plasmid including rck, a
Zhu and Winans
protein implicated in evasion of the host immune response (Ahmer
(1999)
and others 1998). Although the exact role of SdiA in pathogenesis
is unclear, this protein allows EHEC and S. Typhimurium to alter
gene expression in response to the presence of AI-1 produced by
other bacteria (Michael and others 2001).
Cell-to-cell signaling systems are broadly grouped into 4 main

categories. Two of these systems, which use autoinducer-1 (AI-1)
and autoinducer-3 (AI-3), are found in Gram-negative cells, while
the Gram-positive bacteria use a 3rd type of signaling system, the
autoinducing polypeptide (AIP) system. These are primarily involved in intraspecies communication (Smith and others 2004).
The 4th system, using autoinducer-2 (AI-2), is found in Grampositive as well as Gram-negative bacteria. Quorum sensing using
AI-2 is used for interspecies communication (Schauder and others 2001). All of these systems begin with production and release
of autoinducer into the environment by the bacteria. The detection of these chemically distinct autoinducers, and the resulting
alteration in gene expression, is specific to each system.
Autoinducer-1
Autoinducer-2
Many Gram-negative and Gram-positive bacteria possess
quorum-sensing systems that detect an extracellular signal named
AI-2. This signal is synthesized from a by-product of SAM
metabolism. For example, in V. harveyi synthesis of AI-2 is by the
protein LuxS, a synthase encoded by luxS genes. LuxS synthesizes
AI-2 from SAM through a series of steps involving conversion of
ribosehomocysteine into homocysteine and 4,5-dihydroxy-2,3pentanedione (DPD), a compound that cyclizes into several furanones in the presence of water (Schauder and others 2001). The
structure of the 2 AI-2 signals has been determined by cocrystalization with 2 different AI-2-binding proteins: a furanosyl borate
diester (BAI-2) used by V. harveyi to control luminescence and a furanone ([2R,4SL]-2-methyl-2,3,3,4-tetrahydroxytetrahydrofuran
[R-THMF]) used by S. Typhimurium (Miller and others 2004).
AI-2 released by the bacterium accumulates in the cells environment and its detection can be by 2 separate mechanisms. In
the case of V. harveyi, it detects the BAI-2 form of AI-2. This
mechanism detects the presence of AI-2 in the periplasm by first
binding the signal with an autoinducer-specific binding protein,
LuxP. This AI-2/LuxP complex then interacts with a sensor kinase, LuxQ, initiating a phosphotransfer cascade that results in
luciferase production and luminescence. So far, the LuxP/LuxQ
cascade has been identified only in Vibrio spp. AI-2 is handled by
a different mechanism in E. coli and S. Typhimurium. Unlike the
LuxP/LuxQ system, the Lsr (LuxS regulated) system induces a cellular response by transporting AI-2 into the cytoplasm of the cell.
This process starts with recognition of the signal by a periplasmic
protein, LsrB, which binds the R-THMF form of AI-2. Once
bound, the Lsr ABC transporter, comprised of LsrA and LsrC,
imports AI-2 into the cell where LsrK phosphorylates it. The
phosphorylated form of AI-2 interacts with the transcriptional
repressor LsrR to relieve repression of the lsr operon that may
upregulate additional operons in the presence of phosphorylated
AI-2 (Taga and others 2001).
LuxS/AI-2 systems have been discovered in a wide range of
Gram-positive and Gram-negative bacteria leading to the suggestion that the AI-2 system is used for cross-species signaling by
organisms living in mixed-species communities such as biofilms
(Xavier and Bassler 2003).
The LuxIR system was first discovered in Vibrio fisheri during

the investigation of the phenomenon of bioluminesence (Nealson
and others 1970). Now, the LuxI/LuxR system has become the
model system upon that the other quorum-sensing systems have
been based. It consists of LuxI, which synthesizes an N-AHL called
AI-1, and LuxR, a transcription factor responsible for controlling
gene expression in the presence of the autoinducer. LuxI and its
homologues synthesize autoinducers by transferring a fatty acid
chain from an acylated acyl carrier protein (ACP) to SAM, releasing AHL and methylthioadenosine (Schaefer and others 1996).
AHLs produced by LuxI homologues possess different fatty acid
moieties due to recognition of specific ACPs by the synthases and
result in intraspecies and intrageneric signals. Once synthesized,
AI-1 diffuses across the bacterial membrane and is released into
the surrounding environment. With an increase in population, the
concentration of AI-1 in the environment rises. At high population density, the local concentration of AI-1 is high enough to
diffuse back into the cell, where it binds to LuxR. When bound
to AI-1, LuxR activates the transcription of the luxCDABEGH
operon by binding Lux boxes located within the promoter (Devine
and others 1989). The product of this operon, luciferase, catalyzes
a chemical reaction that results in luminescence.
Homologous LuxI/LuxR systems have been identified in many
Gram-negative bacteria, each capable of producing specific AHLs.
In the opportunistic pathogens, such as P. aeruginosa and Serratia
marcescens, these signaling mechanisms control the expression of
the virulence factors. Pseudomonas aeruginosa contains 2 systems
homologous to LuxI/LuxR. LasI/LasR has been shown to con- Autoinducer-3
trol biofilm formation and the production of extracellular enAI-3 employed by the QseC system was first described as a
zymes, as well as transcription of another quorum-sensing system, compound found in spent media that activated the expression of


genes involved in attachment of EHEC to, and subsequent actin
rearrangement in, eukaryotic cells (Sperandio and others 2003).
The structure and synthesis of this signal is still not clear. Early
data suggested that LuxS was involved in AI-3 synthesis, as AI-3
production is impaired in luxS mutants. Further studies, however, proved that the lack of AI-3 production in these mutants
was due to the use of oxaloacetate, instead of SAM, as a precursor for methionine. The addition of L-aspartate to the growth
medium relieved the demand for oxaloacetate, and restored AI-3
production and had no effect on AI-2 production (Walters and
others 2006). This study also found that a number of commensal bacteria such as nonpathogenic EC and Enterobacter cloacae, as
well as pathogenic Shigella, Salmonella, and Klebsiella species, all
produce AI-3. This suggests that AI-3 might represent another
cross-species signal. However, this new signal has not yet been
detected in Gram-positive bacteria.
Detection of AI-3 is accomplished through a 2-component system comprised of the sensor kinase QseC and response regulator
QseB. In the presence of periplasmic AI-3, QseC undergoes autophosphorylation and transfers the phosphate to QseB, which
activates genes responsible for flagella biosynthesis and motility by
upregulating the master flagellar regulator gene flhDC (Clarke and
others 2006). The presence of AI-3 is also linked to the formation
of attaching and effacing lesions by EHEC, a feat accomplished
through upregulation of 5 separate loci of enterocyte effacement
(LEE) operons located within the EHEC chromosome (Sperandio
and others 2003). The complete cascade responsible for regulation
of these genes remains unclear, but likely involves QseA, a LysRfamily regulator that is influenced by cell-to-cell signaling and
directly upregulates LEE genes (Sperandio and others 2002).
Autoinducing Peptides
AIP for cell-to-cell signaling is found exclusively in Grampositive bacteria and are based on the prototypic Agr system first
identified in S. aureus. The Gram-positive bacteria use a polypeptide signal instead of a smaller molecule. The polypeptides produced by the Gram-positive bacteria act as an autoinducer for the
organism that produces it but inhibits other organisms. This signal
is referred to as an AIP and is encoded by the agrD gene. After
translation, the AgrD propeptide is targeted to the membrane by
an N-terminal signal sequence. Once at the membrane, AgrB, a
membrane-bound endopeptidase, cleaves the C-terminus of the
propeptide. The N-terminus of the propeptide, including the signal sequence, is removed by the signal peptidase SpsB. Finally, the
C-terminus of this processed polypeptide is covalently linked to
a conserved, centrally located cysteine to form a thiolactone ring
with a free N-terminal tail. In many cases, both these structures
are required for proper functioning of the AIP. After its release
into the environment, the AIP is recognized by a signal receptor,
AgrC. This protein contains an N-terminal transmembrane domain responsible for recognizing specific AIPs and a C-terminal
histidine kinase domain that, in the presence of the correct AIP,
phosphorylates a response regulator called AgrA. Phosphorylated
AgrA activates transcription of select genes by binding direct repeats located in the promoter regions. One aspect that is unique to
the AIP/Agr system is the fact that an AIP produced by one strain
of Staphylococcus will interfere with another strains Agr system.
This dual role as activator and inhibitor is related to the interaction between the AIP and AgrC. The cyclic structure of AIP is
required for interaction with AgrC, but it is the N-terminal tail
that is responsible for AgrC activation. Removal of this tail, in fact,
results in a universal inhibitor that binds to AgrC but is unable to

activate the Agr system (Lyon and others 2000). The Agr system
has been linked to pathogenesis in many Gram-positive bacteria.
AIP-directed regulation of genes by AgrA results in the production and release of numerous toxins by S. aureus, such as alpha-,
beta-, and delta-hemolysins, serine proteases (SprE), and toxic
shock syndrome toxin 1 (TSST-1) (Parker and Sperandio 2009).
Enterococcus faecalis is another Gram-positive cell that benefits from
the use of AIP signal sensing. This organism uses a 2-component
system homologous to the Agr system of Staphylococcus to detect
the presence of AIP. When AIP is detected, the cell produces and
releases 2 extracellular proteases, gelatinase and SprE (Qin and
others 2000).
Biofilms in Various Food Industries

Biofilms, or in more conventional terms biofouling, are matrixenclosed bacterial populations adhering to each other or to surfaces
or interfaces (Costerton and others 1995). The biofilm community exhibits primitive homeostasis, a primitive circulatory system,
genetic material exchange, and metabolic cooperation (LappinScott and others 1992; Costerton and others 1994, 1995). The
presence of biofilms is highly prevalent and difficult to completely
eliminate. Biofilms can exist on all types of surfaces in food processing plants ranging from plastic, glass, metal, and wood. The
presence of biofilms or attached cells on foods and food contact
surfaces often adversely affects food safety, especially in minimally
processed foods and raw foods (Frank 2001). Elimination of attached pathogens and spoilage microorganisms on minimally processed produces can be difficult because of the hydrophobic cutin,
diverse surface morphologies, and abrasions in the epidermis of
fruits and vegetables (Burnett and Beuchat 2001). The foodborne
pathogens E. coli O157:H7, Listeria monocytogenes, Yersinia enterocolitica, and Campylobacter jejuni are known to form biofilms on food
surfaces and food contact equipment, leading to serious health
problems, and economic losses (Kumar and Anand 1998). Results
from a study of E. coli O157:H7 attachment on apples showed that
the organism attaches to internal core structures or within tissues
of apples and damaged tissues causing its spoilage (Burnett and
others 2000). In another study (Takeuchi and Frank 2000), it was
reported that E. coli O157:H7 prefers to attach to the cut edges
of iceberg lettuce. Pseudomonads, the ubiquitous spoilage organisms are also biofilm formers. They are found in food processing
environments including drains and floors, on fruits, vegetables,
meat surfaces, and in low-acid dairy products (Brocklehurst and
others 1987; Piette and Idziak 1991; Criado and others 1994;
Hood and Zottola 1997). They produce copious amounts of exopolysaccharides and attach and form biofilms on stainless steel
surfaces (Barnes and others 1999) and coexist within biofilms
with Listeria, Salmonella, and other pathogens (Jeong and Frank
1994; Fatemi and Frank 1999; Bagge and others 2001). Bacillus is
found throughout dairy processing plants (Oosthuizen and others 2001). Bacillus and other thermoduric bacteria form biofilms
when hot fluids continuously flow over a surface (Frank 2001).
Spores and vegetative B. cereus cells present in food products can
attach to processing equipment and form biofilms. Salmonella can
be isolated from poultry processing equipment, especially in the
slaughter and evisceration area (Helke and Wong 1994; Joseph and
others 2001). The poultry processing operation is a wet environment and therefore ideal for biofilm formation. Joseph and others
(2001) have shown that Salmonella attach and form biofilms in food
processing plants. Different species of microorganisms may possess
diverse abilities to attach or form biofilms on different surfaces. A
study on the attachment of L. monocytogenes, E. coli O157:H7, and

Pseudomonas fluorescens on iceburg lettuce showed that L. monocytogenes and E. coli O157:H7 attached preferentially to cut edges,
while P. fluorescens attached to intact surfaces (Takeuchi and Frank
2000).
Cells embedded in a biofilm are more resistant to cleaning
agents and other antimicrobial substances, making them difficult to
eradicate from processing equipment (Stoodley and others 2002).
Biofilms on processing equipment surface are a source of contamination for food products due to the continuous detachment of
cells and spores from the biofilm. Moreover, biofilm formation
may cause economic losses due to equipment failure or necessary
extensive cleanup (Kumar and Anand 1998). New biofilm control strategies derived from a better understanding of how bacteria
attach, grow, and detach are urgently needed by the food industry.
Quorum Sensing and Biofilm Formation

Quorum sensing is thought to play a role in the production of
healthy and fully developed biofilms. The complex and multilayer
structures of the defined architecture of the biofilm help the bacterial communities to live in a sessile and protected environment
(OToole and others 2000; Greenberg 2003; Oggioni and others
2006). The formation of biofilms is a multistep process beginning
with microbial surface attachment, cell-to-cell aggregation and
proliferation, exopolysaccharide matrix production, growth, maturation, and, finally, biofilm detachment or degradation (Camara
and others 2002; Yarwood and Schlievert 2003). Quorum-sensing
systems appear to be involved in all phases of biofilm formation.
They regulate the population density and the metabolic activity
within the mature biofilm to fit the nutritional demands and resources available. Bacteria residing within biofilms have markedly
different transcriptional programs from free-living planktonic bacteria of the same strain (Asad and Opal 2008).
Quorum-sensing networks also appear to be instrumental in
the release of bacteria from the extracellular matrix of the biofilm.
The protected sanctuary provided by biofilms presents a problem
of escape from the extracellular matrix in which the bacteria reside. When population densities in biofilms become high, bacteria
are released into the environment. It is suggested that staphylococci use AI-2 signals to reduce the production of polysaccharide
intercellular adhesin and permit the bacteria to escape the biofilm.
Short peptides with detergent qualities that are under quorumsensing control are also deployed to release bacteria for biofilms,
when cell densities are high. Sessile bacteria in biofilms provide a
continuous source of planktonic bacteria as bacterial populations
expand (Novick 2003).
There are several studies that have linked quorum sensing to
biofilm formation in food-related bacteria. Hafnia alvei isolated
from dairy, meat, and fish products is a common bacterial food
contaminant. Hafnia alvei has the potential to form biofilms (Vivas
and others 2008). In a study by Viana and others (2009), AHL
molecules were detected in the biofilms of H. alvei 071. The H.
alvei 071 halI mutant was deficient in biofilm formation. It was
inferred that quorum sensing was required for the differentiation of individual cells of H. alvei 071 into complex multicellular
structures for biofilm formation. In Vibrio cholerae and Serratia liquefaciens, the signaling molecules have been observed to control
exopolymeric substances (EPS) production and control cell aggregation required for biofilm formation, respectively (Gonzalez
Barrios and others 2006). However, van Houdt and others (2004)
found no correlation between biofilm formation and the production of quorum signals in Gram-negative bacteria isolated from
food processing environments. But, it was observed that produc-
tion of quorum signals triggered other biofilm-related responses

such as increased resistance to antimicrobials. Though signaling
molecules have been detected in biofilms, yet their precise role in
biofilm formation is still not clear. Further studies need to be carried out to understand the role played by quorum-sensing signals
in different stages of biofilm formation. Biofilms are a persistent
problem in food processing environment and inhibiting quorum
sensing may eliminate biofilm formation and thus, retard spoilage
and benefit food production and safety (Annous and others 2009).
Quorum-Sensing Signals in Food Spoilage

In recent years, there has been an increasing interest in the
influence of quorum-sensing signaling molecules related to food
spoilage. Various signaling compounds, such as AI-1 and AI-2,
have been detected in different food systems such as milk, meat,
and vegetables (Bruhn and others 2004; Liu and others 2006; Pinto
and others 2007).
Milk and dairy products are easily susceptible to spoilage by
psychrotrophic bacteria such as pseudomonads. These Gramnegative bacteria produce extracellular proteinases, lipases, lecithinases, and glycosidases (Dong and others 2000; Stepaniak 2004),
and the Gram-positive psychrotrophic aerobic Bacillus spp. produce
phospholipases that are responsible for the spoilage of some dairy
products (Stepaniak 2004). In Serratia proteamaculans strainB5a, the
production of extracellular lipolytic and proteolytic enzymes is under the regulon of the AHL-based quorum-sensing system, which
implies the involvement of quorum sensing in the spoilage of
milk by Serratia spp. In an experiment by Christensen and others (2003), the inoculation of pasteurized milk with wild-type S.
proteamaculans caused spoilage after 18 h of storage at room temperature, while the inoculation with a mutant having an inactivated
sprI gene did not result in spoilage. However, the addition of 3oxo-C6-HSL to milk inoculated with the sprI mutant caused its
spoilage, implying the role of signaling molecules in the spoilage of
milk. Similarly, the production of AHLs in both raw and pasteurized milk by the psychrotrophic bacteria Pseudomonas spp., Serratia
spp., Enterobacter spp., and H. alvei shows that quorum sensing may
play a role in the spoilage of milk and dairy products (Whitfield
and others 2000; Pinto and others 2007). Moreover, the detection
of furanosyl BAI-2 signals in significant amounts in regular milk
containing a low bacterial population (102 CFU/mL) suggests
the possible involvement of interspecies communication in milk
spoilage (Lu and others 2004).
Pseudomonas spp. are responsible for the spoilage of meat and
meat products stored under aerobic chill (3 to 8 C) conditions.
Jay and others (2003) have reported the involvement of quorum
sensing in the spoilage process of fresh meat products stored under aerobic refrigerated conditions and in the slime formed on
the meat surfaces. AHL signals, such as C4-HSL, 3-oxo-C6-HSL,
C6-HSL, C8-HSL, and C12-HSL, have been detected in aerobically chill-stored ground beef and chicken by the members of
Pseudomonadaceae (108 to 109 CFU/g) and Enterobacteriaceae (103
to 104 CFU/g) (Liu and others 2006). Hafnia alvei and Serratia spp.
have been identified as the dominating species among the AHLproducing Enterobacteriaceae isolated from vacuum-packed meat,
while Pseudomonas isolates have not produced detectable numbers
of AHL molecules (Ravn and others 2003). In a study by Lu and
others (2004), it was reported that, although the indigenous bacterial population loads were high (6.4 to 8 log CFU/mL), very
low levels of BAI-2 activity (less than onefold induction of luminescence compared with the negative control) was detected in
beef steak, beef patties, chicken breast, and turkey patties. It has


been suggested that the ground beef-derived fatty acids cause the
partial or complete inhibition of AI-2 activity (Soni and others
2008). The cell-free meat extract from spoiled minced pork meat
stored aerobically at refrigerated temperatures contained AHLs
and BAI-2 signals, and the amounts of these signals were higher at
5 C than at 20 C (Ammor and others 2008). Nychas and others
(2007) have demonstrated that the addition of cell-free meat extract to an 18-h culture of P. fluorescens and S. marcescens from fresh
meat increased the lag phase of P. fluorescens and also the metabolic
activity of both the tested strains. Such an increase in metabolic
activity has been linked to the presence of some compounds in
cell-free meat extract, including the quorum-sensing molecules
(Nychas and others 2007). The AHLs have been detected in fresh
ground pork meat stored under a modified atmosphere at 5, 10,
15, and 20 C. AHL production was at its maximum at 10 and
15 C beginning at 7 and 2 d of storage, respectively, and was
associated with the growth of the members of Enterobacteriaceae
and Pseudomonadaceae (Blana and others 2007).
Shewenella putrefaciens and Pseudomonas spp. are the specific
spoilage organisms of iced marine fish and iced freshwater fish, respectively (Gram and others 2002). AHLs have been detected in a
variety of different spoiled commercial fish products, such as coldsmoked salmon, fish fillets, and minced fish. In vacuum-packaged
cold-smoked salmon, spoilage is due to interactions of Enterobacteriaceae and lactic acid bacteria, Carnobacterium sp., and/or Lactobacillus sp., growing to high concentration of 107 to 109 CFU/g
(Jorgensen and others 2000). Gram and others (1999) have shown
that these food spoilage bacteria can produce AHLs even when
they are present at a lower concentration in the food substrate.
The AHLs (mainly 3-oxo-C6-HSL) have been produced by the
inoculated (under conditions that simulated food environments of
5 C, reduced oxygen, and 4% NaCl) and indigenous members of
the Enterobacteriaceae at lower concentrations of 106 CFU/mL and
105 to 106 CFU/g, respectively (Gram and others 1999). A recent
study by Connell (2010) has showed that quorum sensing is modulated in bacteria within low-cell-number/high-density bacterial
clusters and is also affected by population size and the surrounding
medium. This study shows that quorum sensing can be activated
even at much lower concentrations as in food-related situations.
The detection of 3-hydroxy-C8-HSL known to regulate chitinase activity in the nonbioluminescent Photobacterium phosphoreum
and Aeromonas spp. strains isolated from packed cod fillets implies
the possible role of an AHL-based system in the spoilage of crustaceans (Flodgaard and others 2005). The AHLs 3-oxo-C6-HSL,
C6-HSL, C8-HSL, and C12-HSL have been detected in H. alvei,
S. liquefaciens, P. fluorescens, and Pseudomonas putida responsible for
the proteolytic activity and spoilage of rainbow trout fillets. Similar AHL-modulated proteolytic activity has been reported in S.
proteamaculans B5a, a strain originally isolated from cold-smoked
salmon (Christensen and others 2003) suggesting the involvement
of quorum-sensing signals AHLs in food spoilage.
The pectinolytic activity of Pseudomonadaceae or Enterobacteriaceae (mostly Erwinia spp.) growing to high-cell densities (108 to
109 CFU g/L) in fruits and vegetables causes enzymatic browning,
off-tastes, off-odors, and/or texture breakdown resulting in their
spoilage (Liao 1989). Erwinia and Pseudomonas produce various
pectinolytic enzymes, namely, pectin lyases, pectate lyase, polygalacturonase, and pectin methyl esterases, which are responsible
for the spoilage of ready-to-eat vegetables, also produce a broad
range of AHLs (mainly 3-oxo-C6-HSL and C6-HSL) (Rasch
and others 2005). This suggests the involvement of AHL-based
quorum-sensing systems in the spoilage of vegetables and fruits.

Moreover, inoculation of bean sprouts with AHL-producing pectinolytic Pectobacterium carotovorum increased the rate of its spoilage
(Rasch and others 2005). In P. carotovorum subsp. Carotovorum, the
production of extracellular enzymes pectate lyase, pectin lyase,
polygalacturonase, cellulase, and protease is regulated by 3-oxoC6-HSL-dependent quorum sensing (Pirhonen and others 1993).
These data provide evidence that the bacterial spoilage of some
food products is influenced by quorum-sensing-regulated phenotypes. In Serratia plymouthica RVH1, a strain isolated from a raw
vegetable processing line, a LuxI homolog, SplI, controls the production of the 3 AHLs, C4-HSL, C6-HSL, and 3-oxo-C6-HSL,
whose inactivation resulted in the complete loss of 3-oxo-C6HSL production and decrease in C4-HSL and C6-HSL production. SplI-dependent quorum sensing is involved in the production
of extracellular chitinase, nuclease, protease, and an antibacterial
compound and 2,3-butanediol fermentation (van Houdt and others 2006). The production of these exoenzymes in RVH1 was
reduced in the splI mutant and was restored only by the addition of C6-HSL or 3-oxo-C6-HSL (van Houdt and others 2007).
In the cucumber rot-associated S. marcescens strain MG1 and in
Serratia sp. ATCC 39006 the secretion of extracellular enzymes
involved in spoilage of vegetables is regulated by the SwrI/SwrR
quorum-sensing system and its cognate C4-HSL and SmaI/SmaR
QS system and its cognate C4-HSL and C6-HSL, respectively
(Thomson and others 2000; Riedel and others 2001; van Houdt
and others 2006).
Thus, from the above studies, it is clear that AHL-based
quorum-sensing systems in Gram-negative bacteria are extensively associated with food spoilage. In table 2, food spoilage of
various food products influenced by quorum-sensing-regulated
traits is listed. However, there is scarce information on AI-2 and
none about the AIPs produced by Gram-positive bacteria in food
spoilage. Moreover, the presence of quorum-sensing signaling
compounds in pasteurized milk and in meat and fish products
that are refrigerated, vacuum-packaged, and under modified atmosphere clearly reveals that the existing preservative techniques
are inadequate. Knowledge of the types of spoilage microbes and
their quorum-sensing systems in the various categories of food
products will help in developing quorum-sensing inhibitors that
can then be used as novel food preservatives.
Detection of Quorum-Sensing Signals in Food Using

Biosensors
Quorum-sensing signaling molecules can be detected from cellfree supernatants, extracts of food samples, and spent culture supernatants of bacteria isolated from food products (Ammor and
others 2008).
AHLs have been identified and quantified and their structures
elucidated using mass spectrometry (MS), high-performance liquid chromatography-MS, gas chromatography-MS, and nuclear
magnetic resonance spectroscopy (Throup and others 1995; Schaefer and others 2000; Cataldi and others 2007). However, the use
of bacterial biosensors has made the detection and quantification
of different types of AHLs easier, economical, and faster. The
biosensors contain a functional LuxR family protein cloned with
a cognate target promoter (usually the promoter of the cognate
luxI synthase), which upregulates the expression of a reporter gene
encoding for a phenotypic response only in the presence of exogenous AHLs, as they do not produce the signaling molecules but
only possess their cognate receptors (Steindler and Venturi 2007).
Using the reporter strains, the AHLs can be detected either on
agar or in the spent culture supernatant. The investigated strain is

Table 2Bacterial food spoilage influenced by quorum-sensing-regulated phenotypes.
Organism
Food product
Pseudomonas fluorescens 395

Serratia proteomaculans strainB5a
Milk
Milk
Pseudomonas fluorescens
Signal-dependent
phenotype
Signaling
molecules
Milk
L-HSL -amino- -butyrolactones
Pseudomonas phosphoreum and

Aeromonas spp.
Erwinia carotovora
Cod fillets
Chitinolytic activity
3-hydroxy-C8-HSL
Vegetables
3-oxo-C6- HSL
Pectobacterium sp. A2JM
Bean sprouts
3-oxo-C6- HSL
Rasch and others (2005)
Serratia plymuthica RVH1
Vegetables
3-oxo-C6- HSL and C6-HSL
Hafnia alvei and Serratia spp.
Vaccum packed
meat
Meat
Cellulolytic and proteolytic

spoilage
Pectinolytic and proteolytic
spoilage
Chitinase and protease
activity
Proteolytic spoilage
Liu and others (2007)

Christensen and others
(2003)
Dunstall and others
(2005)
Flodgaard and others
(2005)
Jones and others (1993)
Van Houdt and others

(2007)
Bruhn and others
(2004)
Jay and others (2003)
Pseudomonas spp.
Photobacterium phosphoreum and
Aeromonas spp.
Cod fillets
Biofilm formation and

proteolytic spoilage
Chitinolytic spoilage
cross-streaked close to the biosensor on an appropriate agar

medium. The production of AHLs by the test strain will activate
the expression of the reporter gene encoding for the phenotypic
response. This results in a gradient of responses that can be observed at the meeting point of the 2 strains (Steindler and Venturi
2007).
The AHLs from spent supernatants of late exponential phase
cultures can be extracted using the solvents dichloromethane, ethyl
acetate, or chloroform. The bacterial extracts are separated by
thin-layer chromatography (TLC) on C18 reversed phase plates,
and then inoculated with the biomonitor systems. The biosensing
of exogenous AHL results in the formation of a spot, which is
identified according to the AHL standards included in the assay
(McClean and others 1997; Schaefer and others 2000; Turovskiy
and others 2007) and further detected using analytical techniques
(Shaw and others 1997).
Burmolle and others (2003) developed an approach for detecting AHL production using a whole-cell biosensor. The regulatory
region of the lux-operon from Vibrio fischeri was fused to green fluorescent protein (gfp) resulting in a luxR-PluxI-gfpmut3-fusion
in the high copy plasmid, pAHL-GFP. EC MC4100 harboring the
pAHL-GFP responded to the AHL-compound N-octanoyl homoserine lactone (OHL) by expressing green fluorescence. The
induced cells were then verified by single-cell analysis using flow
cytometry. Using this biosensor, OHL concentrations between 0.5
and 50 nmol/g soil were detected in soil samples. When AHLproducing S. liquefaciens was introduced to soil microcosms, expression of gfp was induced in EC MC4100/pAHL-GFP. Thereby, the
ability of this strain to detect excretion of AHLs by S. liquefaciens
in sterile soil was shown. Thus, the biosensor strains containing
the genes encoding GFP can be used in the T-streak and TLC
assays, and epifluorescent microscopes can be used to detect the
GFP emission. These biosensors can also be combined with a flow
cytometer for the detection of AHLs.
The bioassays recognize only known compounds and require
the use of many reporters for different kinds of AHL molecules.
The reporter strains display a high specificity toward the cognate AHL and to a lesser extent to closely related ones. Thus,
the detection of a wide range of AHLs requires the use of several biosensors, each responding to AHLs with different structural
features.
There are some reporter strains that lack specificity. The TraR
of A. tumefaciens, sensitive to most 3-oxo-HSLs (Shaw and oth-
C4-HSL and 3OC8-HSL

3-oxo-C6- HSL
References
Proteolytic milk spoilage

Lipolytic and proteolytic milk
spoilage
Proteolytic milk spoilage
N-3-oxohexanoyl HSL
AHLs
3-hydroxy-C8-HSL
Flodgaard and others

(2005)
ers 1997) and the V. fischeri LuxR-based reporter plasmids such

as pSB403, activated by AHLs with carbon chains of C6 or C8
with or without 3-oxo substitutions (Winson and others 1998)
are examples of reporter strains lacking in specificity. Using these
biosensors can lead to false-positive and false-negative reactions.
Moreover, the screened bacterium might produce non-AHL compounds that could potentially interfere or activate the response of
biosensors (Holden and others 1999). As different LuxR homologues have diverse affinities with different AHLs, it is not accurate to compare the intensity of a response obtained with different
AHLs. Therefore, synthetic AHL must be used to determine the
minimal amount of AHL required for a response and the amount
necessary for a saturated response to plot the linear dose-response
curve (Steindler and Venturi 2007). The high degree of diversity
among LuxI and LuxR homologue proteins has become a limiting factor for the development of molecular methods for their
easy identification (Whitehead and others 2001).
AI-2 is detected using the biosensor V. harveyi BB170
luxN::Tn5 that synthesizes all 3 autoinducers, HAI-1 (3OHC4HSL), an AHL; AI-2, a furanosyl-borate-diester; and Cholerae
Autoinducer-1 [CAI-1, an (S)-3-hydroxytridecan-4-one], of unknown structure but senses only AI-2 (Henke and Bassler 2004).
BAI-2 activity is calculated as the ratio of luminescence of the test
sample to that of the control (negative) sample and expressed as
relative activity. The instability of the AI-2 molecule makes the
application of chemical methods difficult. Thus, bioassay seems to
be the only mode of AI-2 detection. The growth and ability of the
biosensor to detect BAI-2 is influenced by the components of the
culture medium and the components and additives in food sometimes leading to false-negative or false-positive results (Lu and others 2004). For example, the luciferase in V. harveyi is permanently
repressed by glucose through catabolite repression, and despite the
presence of the luxS gene, no BAI-2 activity can be detected.
Low pH also affects bioluminescence, making it necessary to adjust the pH of culture supernatants to 7.0 before bioassay testing (de Keersmaecker and Vanderleyden 2003). The effect of all
these factors makes the BAI-2 bioassay only qualitative in nature
(Turovskiy and Chikindas 2006). Currently, the quantification of
BAI-2 is carried out using a LuxP- fluorescence resonance energy transfer (FRET) based reporter strain. The sensor is based on
ligand binding-induced changes in FRET between a cyan variant and yellow variant of GFP fused to the termini of the BAI-2
receptor, LuxP (Rajamani and others 2007).


The AI-3 molecule is detected by the -galactosidase assay
using the E. coli O157:H7 TEVS232 strain (Sperandio and others
2000) in which the LEE1 regulatory regions are fused to the lacZ
reporter gene in TE2680. TEVS232 is grown in fresh medium or
in medium supplemented with Pseudomonas cepacia. Cultures are
diluted 1:10 in Z buffer, and -galactosidase activity is measured by
using o-nitrophenyl -D-galactopyranoside as a substrate (Walters
and others 2006).
Methods for the detection and quantification of AIPs mainly
involve the application of nisin. The bioassays based on nisininducible bioluminescence (Wahlstrom and Saris 1999; Immonen and Karp 2007) and fluorescence (Reunanen and Saris 2003;
Hakovirta and others 2006) involve reporter genes placed under
the control of a nisin-inducible promoter, either bacterial luciferase
genes (lux) or the GFP gene (gfp). The GFP-based nisin microplate
bioassay uses an L. lactis strain, LAC275, which chromosomally encodes the nisin regulatory proteins NisK and NisR and a plasmid
with a GFP variant gene, gfpuv , under the control of the nisininducible nisA promoter. This strain is capable of transducing the
signal from extracellular nisin into measurable GFPuv fluorescence
through the NisRK signal transduction system. The sensitivity of
this biosensor is quite high and it can detect nisin concentrations
upto of 10 pg/mL in culture supernatant, 0.2 ng/mL in milk, 3.6
ng/g in processed cheese, 1 ng/g in salad dressings and crushed
canned tomatoes, and 2 ng/g in liquid egg (Hakovirta and others 2006). However, autofluorescence of the cellular background
lowers the sensitivity (Hakkila and others 2002). Before measuring
the fluorescence, supernatant must be removed as it absorbs light
at the same wavelengths as GFP (Immonen and Karp 2007).
2-Alkyl-4-quinolones (AHQs) and 2-heptyl-4-quinolone of
the Pseudomonas spp. are detected and quantified using the luxbased P. aeruginosa AHQ biosensor strain (Fletcher and others
2007). In this method, the reporter strain is used either in TLC or
microtiter plate assays, wherein the bioluminescence or the green
color of pyocyanin is detected as end points. In the TLC assay, the
bacterial extracts or cell free supernatant are separated on TLC
plates. The dried TLC plates are overlaid with the AHQ biosensor. AHQs if present are seen as luminescent green spots. In the
microtiter assay, bacterial extracts or CFS are added to a growth
medium containing the AHQ biosensor and the resulting light is
proportional to the AHQ content of the sample.
Quorum-Sensing Inhibitors in Food Preservation

The involvement of AHLs in the regulation of virulence factors in several opportunistic human and plant pathogenic bacteria
has paved the way for an intense search of compounds that can
specifically block AHL communication. In the clinical scenario,
it is envisioned that such compounds can block expression of
virulence without affecting growth and also decrease the risk of
resistance development. Quorum-sensing inhibitors are typically
analogues of the AHLs (Eberhard and others 1986), or compounds
that degrade AHLs (Dong and others 2000). A promising group of
quorum-sensing inhibitors is the halogenated furanones produced
by the Australian red alga, Delisea pulchra (Givskov and others
1996). These interfere with the receptor proteins and release the
AHL signal (Manefield and others 1999, 2002). Treatment with
these compounds has reduced the expression of AHL-regulated
virulence factors and biofilm formation in P. aeruginosa and S. liquefaciens (Givskov and others 1996; Rasmussen and others 2000;
Hentzer and others 2002). The cytotoxicity and chemically unstable nature of these halogenated furanones has prompted the

screening of nontoxic quorum-sensing inhibitors from natural

sources. Plants used in traditional medicine are one of the most
promising areas in the search for new biologically active compounds (Hullati and Rai 2004; Jamuna Bai and others 2011). In a
study by Vattem and others (2007), dietary phytochemicals from
plants known to have several health benefits and antimicrobial
activity, exhibited quorum-sensing inhibitory activity at sublethal
concentrations. The bioactive dietary phytochemical extracts from
common dietary fruit, herb, and spice extracts significantly inhibited quorum sensing in Chromobacterium violaceum O26 (CVO26)
and CV 31532. The extracts also inhibited swarming motility in
pathogens EC O157:H7 and P. aeruginosa (PA-01), known to be
modulated by quorum sensing. Vanilla, a widely used spice and
flavor, can inhibit bacterial quorum sensing. The extract of vanilla
beans in the C. violaceum CV026 bioassay effectively inhibited
bacterial quorum sensing. Vanilla extract, or specific compounds
isolated from it, may be used as novel quorum-sensing inhibitor.
These will have a greater advantage for human use than the toxic
furanone compounds, as vanilla has been used safely for a long
time (Choo and others 2006). Girennavar and others (2008) have
reported that natural furocoumarins from grapefruit juice act as the
potent inhibitors of AI-1 and AI-2 activity and biofilm formation
in S. Typhimurium, EC, and P. aeruginosa. These results suggest
that grapefruit juice can serve as a safe source of alternatives to the
halogenated furanones to develop strategies targeted at microbial
quorum sensing. Thus, quorum-sensing inhibitors can also be used
as food preservatives in selected foods where AHL-regulated traits
are responsible for food spoilage. The finding of quorum-sensing
inhibitory compounds from plants raises the possibility of identifying active quorum-sensing inhibitory compounds from a plethora
of natural sources. Quorum-sensing inhibitors may prevent colonization of food surfaces, toxin formation, and proliferation of
food-related bacteria. The natural occurrence of quorum-sensing
inhibitors is an important consideration for the assessment of their
toxicological status and may facilitate their use in food as preservatives and hence pave way for the application of novel food
preservation techniques.
Conclusion
Food spoilage, a consequence of intrinsic biochemical changes
and microbial activities, is a complex process. Recent studies have
provided evidence that quorum sensing, which was earlier implicated in microbial virulence and pathogenesis, may also play a role
in food spoilage. AHL- and AI-2-based quorum-sensing systems
associated with Gram-negative bacteria in different food ecosystems have been detected. Further studies have to be carried out
to know if AIPs of Gram-positive bacteria have a potential role
in food spoilage. Although quorum-sensing signaling molecules
have been detected in spoiled foods, the exact role played by them
in food spoilage is still not clear. Understanding the mechanism
of quorum-sensing systems in food ecosystems can help in targeting quorum sensing and addressing the problem of food spoilage.
Quorum-sensing inhibitors could be used as food preservatives to
enhance food safety and increase shelf life.
Acknowledgments
The authors gratefully acknowledge Dr. K.S. Manja, Former
Director, Defence Research and Development Organization, for
critically reviewing and providing constructive suggestions for improving the manuscript.

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Bacterial Quorum Sensing and Food Industry

A. Jamuna Bai and V. Ravishankar Rai

cell communication is employed by a diverse group of bacteria

Food spoilage is a complex process. It is caused by the various

Bacterial quorum sensing . . .

Mechanisms of Quorum Sensing

systems are used in modulating the target gene expression. One

Bacterial quorum sensing . . .

RhlI/RhlR, adding an additional level of control through AHL

Cell-to-cell signaling systems are broadly grouped into 4 main

The LuxIR system was first discovered in Vibrio fisheri during

Bacterial quorum sensing . . .

Biofilms in Various Food Industries

Bacterial quorum sensing . . .

Quorum Sensing and Biofilm Formation

tion of quorum signals triggered other biofilm-related responses

Quorum-Sensing Signals in Food Spoilage

Bacterial quorum sensing . . .

Detection of Quorum-Sensing Signals in Food Using

Bacterial quorum sensing . . .

Pseudomonas fluorescens 395

L-HSL -amino- -butyrolactones

Pseudomonas phosphoreum and

Pectobacterium sp. A2JM

Rasch and others (2005)

Serratia plymuthica RVH1

3-oxo-C6- HSL and C6-HSL

Hafnia alvei and Serratia spp.

Cellulolytic and proteolytic

Liu and others (2007)

Van Houdt and others

Biofilm formation and

cross-streaked close to the biosensor on an appropriate agar

C4-HSL and 3OC8-HSL

Proteolytic milk spoilage

Flodgaard and others

ers 1997) and the V. fischeri LuxR-based reporter plasmids such

Bacterial quorum sensing . . .

Quorum-Sensing Inhibitors in Food Preservation

screening of nontoxic quorum-sensing inhibitors from natural

Bacterial quorum sensing . . .

de Keersmaecker SC, Vanderleyden J. 2003. Constraints on detection of

Bacterial quorum sensing . . .

Manefield M, Rasmussen TB, Hentzer M, Andersen JB, Steinberg P,

Bacterial quorum sensing . . .

Serratia is under quorum sensing control. Mol Microbiol 36:539

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